Semin Respir Crit Care Med 2007; 28(5): 475-485
DOI: 10.1055/s-2007-991520
© Thieme Medical Publishers

Technical Aspects of Bronchoalveolar Lavage: Recommendations for a Standard Procedure

Robert P. Baughman1
  • 1Division of Pulmonary and Critical Care Medicine, University of Cincinnati Medical Center, Cincinnati, Ohio
Further Information

Publication History

Publication Date:
02 November 2007 (online)

ABSTRACT

Bronchoalveolar lavage (BAL) has been used widely in the diagnosis of infection. More than 30 years after its description, its use in the clinical management of interstitial lung disease remains controversial. One limitation has been the variations in how the specimen is obtained and handled. Several groups have developed recommendations for obtaining and handling BAL specimens. This article summarizes these recommendations and discusses the variable effects they have on BAL results. The final recommendations provide a standard methodology that can be used by the largest number of pulmonologists.

REFERENCES

  • 1 Reynolds H Y, Newball H H. Analysis of proteins and respiratory cells obtained from human lungs by bronchial lavage.  J Lab Clin Med. 1974;  84 559-573
  • 2 Reynolds H Y. Use of bronchoalveolar lavage in humans: past necessity and future imperative.  Lung. 2000;  178 271-293
  • 3 Baughman R P. The uncertainties of bronchoalveolar lavage.  Eur Respir J. 1997;  10 1940-1942
  • 4 Klech H, Haslam P, Turner-Warwick M. Worldwide clinical survey on bronchoalveolar lavage (BAL) in sarcoidosis: experience in 62 centers in 19 countries: preliminary analysis.  Sarcoidosis. 1986;  3 113-117
  • 5 Klech H, Pohl W. Technical recommendations and guidelines for bronchoalveolar lavage (BAL).  Eur Respir J. 1989;  2 561-585
  • 6 Haslam P L, Baughman R P. ERS task force report on measurement of acellular components in BAL.  Eur Respir Rev. 1999;  9 25-27
  • 7 King Jr T E. The handling and analysis of bronchoalveolar lavage specimens. In: Baughman RP Bronchoalveolar Lavage. St. Louis, MO; Mosby Year Book 1992: 3-25
  • 8 The BAL Cooperative Group Steering Committee . Bronchoalveolar lavage constituents in healthy individuals, idiopathic pulmonary fibrosis, and selected comparison groups.  Am Rev Respir Dis. 1990;  141 S169-S202
  • 9 Bronchoalveolar lavage constituents in healthy individuals, idiopathic pulmonary fibrosis, and selected comparison groups. The BAL Cooperative Group Steering Committee.  Am Rev Respir Dis. 1990;  141 S169-S202
  • 10 Garcia J G, Wolven R G, Garcia P L, Keogh B A. Assessment of interlobar variation of bronchoalveolar lavage cellular differentials in interstitial lung diseases.  Am Rev Respir Dis. 1986;  133 444-449
  • 11 Baughman R P, Dohn M N, Shipley R, Buchsbaum J A, Frame P T. Increased Pneumocystis carinii recovery from the upper lobes in Pneumocystis pneumonia. The effect of aerosol pentamidine prophylaxis.  Chest. 1993;  103 426-432
  • 12 Martin T R, Raghu G, Maunder R J, Springmeyer S C. The effects of chronic bronchitis and chronic bronchial air-flow obstruction on lung cell populations recovered by bronchoalveolar lavage.  Am Rev Respir Dis. 1985;  132 254-260
  • 13 Baughman R P. Asthma and other diseases. In: Baughman RP Bronchoalveolar Lavage. St. Louis; Mosby Year Book 1992: 244-262
  • 14 Metzger W J, Zavala D, Richerson H B. Local allergen challenge and bronchoalveolar lavage of allergic asthmatic lungs.  Am Rev Respir Dis. 1987;  135 433-440
  • 15 Metzger W J, Neugent K, Richardson H B et al.. Methods of bronchoalveolar lavage in asthmatic patients following bronchoprovocation and local antigen challenge.  Chest. 1985;  87S 16S-17S
  • 16 National Institutes of Health workshop summary: summary and recommendations of a workshop on the investigative use of fiberoptic bronchoscopy and bronchoalveolar lavage in individuals with asthma.  J Allergy Clin Immunol. 1985;  76 145-147
  • 17 Van V T, Chanez P, Bousquet J, Lacoste J Y, Michel F B, Godard P. Safety of bronchoalveolar lavage and bronchial biopsies in patients with asthma of variable severity.  Am Rev Respir Dis. 1992;  146 116-121
  • 18 Elston W J, Whittaker A J, Khan L N et al.. Safety of research bronchoscopy, biopsy and bronchoalveolar lavage in asthma.  Eur Respir J. 2004;  24 375-377
  • 19 Mancini N M, Bene M C, Gerard H et al.. Early effects of short-time cigarette smoking on the human lung: a study of bronchoalveolar lavage fluids.  Lung. 1993;  171 277-291
  • 20 Baughman R P, Gunther K L, Rashkin M C, Keeton D A, Pattishall E N. Changes in the inflammatory response of the lung during acute respiratory distress syndrome: prognostic indicators.  Am J Respir Crit Care Med. 1996;  154 76-81
  • 21 Steinberg K P, Mitchell D R, Maunder R J, Milberg J A, Whitcomb M E, Hudson L D. Safety of bronchoalveolar lavage in patients with adult respiratory distress syndrome.  Am Rev Respir Dis. 1993;  148 556-561
  • 22 Guerra L F, Baughman R P. Use of bronchoalveolar lavage to diagnose bacterial pneumonia in mechanically ventilated patients.  Crit Care Med. 1990;  18 169-173
  • 23 Baughman R P. How I do bronchoalveolar lavage.  J Bronchology. 2003;  10 309-314
  • 24 Kelly C, Ward C, Bird G, Hendrick D, Walters H. The effect of filtration on absolute and differential cell counts in fluid obtained at bronchoalveolar lavage.  Respir Med. 1989;  83 107-110
  • 25 Schaberg T, Lauer C, Lode H, Fischer J, Haller H. Increased number of alveolar macrophages expressing adhesion molecules of the leukocyte adhesion molecule family in smoking subjects: association with cell-binding ability and superoxide anion production.  Am Rev Respir Dis. 1992;  146 1287-1293
  • 26 Mordelet-Dambrine M, Arnoux A, Stanislas-Leguern G, Sandron D, Chretien J, Huchon G. Processing of lung lavage fluid causes variability in bronchoalveolar cell count.  Am Rev Respir Dis. 1984;  130 305-306
  • 27 Dohn M N, Baughman R P. Effect of changing instilled volume for bronchoalveolar lavage in patients with interstitial lung disease.  Am Rev Respir Dis. 1985;  132 390-392
  • 28 Davis G S, Giancola M S, Costanza M C, Low R B. Analysis of sequential bronchoalveolar lavage samples from healthy human volunteers.  Am Rev Respir Dis. 1982;  126 611-616
  • 29 Merrill W, O'Hearn E, Rankin J, Naegel G, Matthay R A, Reynolds H Y. Kinetic analysis of respiratory tract proteins recovered during a sequential lavage protocol.  Am Rev Respir Dis. 1982;  126 617-620
  • 30 Helmers R A, Dayton C S, Floerchinger C, Hunninghake G W. Bronchoalveolar lavage in interstitial lung disease: effect of volume of fluid infused.  J Appl Physiol. 1989;  67 1443-1446
  • 31 Rennard S I, Ghafouri M, Thompson A B et al.. Fractional processing of sequential bronchoalveolar lavage to separate bronchial and alveolar samples.  Am Rev Respir Dis. 1990;  141 208-217
  • 32 Thompson A B, Bohling T, Payvandi F, Rennard S I. Lower respiratory tract lactoferrin and lysozyme arise primarily in the airways and are elevated in association with chronic bronchitis.  J Lab Clin Med. 1990;  115 148-158
  • 33 Dohn M N, Baughman R P. Effect of changing instilled volume for bronchoalveolar lavage in patients with interstitial lung disease.  Am Rev Respir Dis. 1985;  132 390-392
  • 34 Cole P, Turton C, Lanyon H, Collins J. Bronchoalveolar lavage for the preparation of free lung cells: technique and complications.  Br J Dis Chest. 1980;  74 273-278
  • 35 Cantin A, Begin R, Rola-Pleszczynski M, Boileau R. Heterogeneity of bronchoalveolar lavage cellularity in stage III pulmonary sarcoidosis.  Chest. 1983;  83 485-486
  • 36 Clements P J, Goldin J G, Kleerup E C et al.. Regional differences in bronchoalveolar lavage and thoracic high-resolution computed tomography results in dyspneic patients with systemic sclerosis.  Arthritis Rheum. 2004;  50 1909-1917
  • 37 DeSantis M, Bosello S, LaTorre G et al.. Functional, radiological and biological markers of alveolitis and infections of the lower respiratory tract in patients with systemic sclerosis.  Respir Res. 2005;  6 96
  • 38 O'Roirdan T G, Baughman R P, Dohn M N, Smalldone G C. Lobar pentamidine levels and Pneumocystis carinii pneumonia following aerosolized pentamidine.  Chest. 1994;  105 53-56
  • 39 Levine S J, Masur H, Gill V J et al.. Effect of aerosolized pentamidine prophylaxis on the diagnosis of Pneumocystis carinii pneumonia by induced sputum examination in patients infected with the human immunodeficiency virus.  Am Rev Respir Dis. 1991;  144 760-764
  • 40 Cole P, Turton C, Lanyon H, Collins J. Bronchoalveolar lavage for the preparation of free lung cells: technique and complications.  Brit J Dis Chest. 1980;  74 273-278
  • 41 Baughman R P, Spencer R E, Kleykamp B O, Rashkin M C, Douthit M M. Ventilator associated pneumonia: quality of nonbronchoscopic bronchoalveolar lavage sample affects diagnostic yield.  Eur Respir J. 2000;  16 1152-1157
  • 42 Baughman R P, Rennard S I. Bronchoalveolar lavage sampling and general approaches to correction for variability of dilution and lung permeability.  Eur Respir Rev. 1999;  9 28-31
  • 43 Rennard S I, Basset G, Lecossier D, O'Donnell K, Martin P, Crystal R G. Estimation of volume of epithelial lining fluid recovered by lavage using urea as marker of dilution.  J Appl Physiol. 1986;  60 532-538
  • 44 Marcy T W, Merrill W, Rankin J A, Reynolds H Y. Limitations of using urea to quantify epithelial lining fluid recovered by bronchoalveolar lavage.  Am Rev Respir Dis. 1987;  135 1276-1280
  • 45 Kelly C A, Fenwick J D, Corris P A, Fleetwood A, Hendrick D J, Walters E H. Fluid dynamics during bronchoalveolar lavage.  Am Rev Respir Dis. 1988;  138 81-84
  • 46 Baughman R P. The uncertainties of bronchoalveolar lavage.  Eur Respir J. 1997;  10 1940-1942
  • 47 Baughman R P, Bosken C H, Loudon R G, Hurtubise P, Wesseler T. Quantitation of bronchoalveolar lavage with methylene blue.  Am Rev Respir Dis. 1983;  128 266-270
  • 48 Cantral D E, Tape T G, Reed E C, Spurzem J R, Rennard S I, Thompson A B. Quantitative culture of bronchoalveolar lavage fluid for the diagnosis of bacterial pneumonia.  Am J Med. 1993;  95 601-607
  • 49 Thorpe J E, Baughman R P, Frame P T, Wesseler T A, Staneck J L. Bronchoalveolar lavage for diagnosing acute bacterial pneumonia.  J Infect Dis. 1987;  155 855-861
  • 50 Rankin J A, Naegel G P, Reynolds H Y. Use of a central laboratory for analysis of bronchoalveolar lavage fluid.  Am Rev Respir Dis. 1986;  133 186-190
  • 51 Baughman R P, Drent M. Role of bronchoalveolar lavage in interstitial lung disease.  Clin Chest Med. 2001;  22 331-341
  • 52 Cobben N A, Jacobs J A, Dieijen-Visser M P, Mulder P G, Wouters E F, Drent M. Diagnostic value of BAL fluid cellular profile and enzymes in infectious pulmonary disorders.  Eur Respir J. 1999;  14 496-502
  • 53 Drent M, Jacobs J A, Cobben N A, Costabel U, Wouters E F, Mulder P G. Computer program supporting the diagnostic accuracy of cellular BALF analysis: a new release.  Respir Med. 2001;  95 781-786
  • 54 Drent M, Mulder P G, Wagenaar S S, Hoogsteden H C, van Velzen Blad H, van den Bosch J M. Differences in BAL fluid variables in interstitial lung diseases evaluated by discriminant analysis.  Eur Respir J. 1993;  6 803-810
  • 55 Kantrow S P, Meyer K C, Kidd P, Raghu G. The CD4/CD8 ratio in BAL fluid is highly variable in sarcoidosis.  Eur Respir J. 1997;  10 2716-2721
  • 56 Winquist A G, Orrico M A, Peterson L R. Evaluation of the cytocentrifuge Gram stain as a screening test for bacteriuria in specimens from specific patient populations.  Am J Clin Pathol. 1997;  108 515-524
  • 57 Armbruster C, Pokieser L, Hassl A. Diagnosis of Pneumocystis carinii pneumonia by bronchoalveolar lavage in AIDS patients: comparison of Diff-Quik, fungifluor stain, direct immunofluorescence test and polymerase chain reaction.  Acta Cytol. 1995;  39 1089-1093
  • 58 De Brauwer E I, Jacobs J A, Nieman F, Bruggeman C A, Wagenaar S S, Drent M. Cytocentrifugation conditions affecting the differential cell count in bronchoalveolar lavage fluid.  Anal Quant Cytol Histol. 2000;  22 416-422
  • 59 Fleury-Feith J, Escudier E, Pocholle M J, Carre C, Bernaudin J F. The effects of cytocentrifugation on differential cell counts in samples obtained by bronchoalveolar lavage.  Acta Cytol. 1987;  31 606-610
  • 60 De Brauwer E I, Drent M, Mulder P G, Bruggeman C A, Wagenaar S S, Jacobs J A. Differential cell analysis of cytocentrifuged bronchoalveolar fluid samples affected by the area counted.  Anal Quant Cytol Histol. 2000;  22 143-149
  • 61 Willcox M, Kervitsky A, Watters L C, King Jr T E. Quantification of cells recovered by bronchoalveolar lavage: comparison of cytocentrifuge preparations with the filter method.  Am Rev Respir Dis. 1988;  138 74-80
  • 62 Saltini C, Hance A J, Ferrans V J, Basset F, Bitterman P B, Crystal R G. Accurate quantification of cells recovered by bronchoalveolar lavage.  Am Rev Respir Dis. 1984;  130 650-658
  • 63 Laviolette M, Carreau M, Coulombe R. Bronchoalveolar lavage cell differential on microscope glass cover: a simple and accurate technique.  Am Rev Respir Dis. 1988;  138 451-457
  • 64 Thompson A B, Teschler H, Wang Y M, Konietzko N, Costabel U. Preparation of bronchoalveolar lavage fluid with microscope slide smears.  Eur Respir J. 1996;  9 603-608
  • 65 Rennard S I. Bronchoalveolar lavage in the diagnosis of cancer.  Lung. 1990;  168(Suppl) 1035-1040
  • 66 Tollerud D J, Wesseler T A, Kim C K, Baughman R P. Use of a rapid differential stain for identifying Pneumocystis carinii in bronchoalveolar lavage fluid: diagnostic efficacy in patients with AIDS.  Chest. 1989;  95 494-497
  • 67 Robinson-Smith T M, Saad A, Baughman R P. Interpretation of the Wright-Giemsa stained bronchoalveolar lavage specimen.  Laboratory Medicine. 2004;  35 553-557
  • 68 Moumouni H, Garaud P, Diot P, Lemarie E, Anthonioz P. Quantification of cell loss during bronchoalveolar lavage fluid processing: effects of fixation and staining methods.  Am J Respir Crit Care Med. 1994;  149 636-640
  • 69 Xaubet A, Moises J A, Agusti C, Martos J A, Picado C. Identification of mast cells in bronchoalveolar lavage fluid: comparison between different fixation and staining methods.  Allergy. 1991;  46 222-227
  • 70 De Brauwer E I, Jacobs J A, Nieman F, Bruggeman C A, Drent M. Bronchoalveolar lavage fluid differential cell count: how many cells should be counted?.  Anal Quant Cytol Histol. 2002;  24 337-341
  • 71 Baughman R P, Strohofer S, Colangelo G, Frame P T. Semiquantitative technique for estimating Pneumocystis carinii burden in the lung.  J Clin Microbiol. 1990;  28 1425-1427
  • 72 Baughman R P, Golden J A, Keith F M. Bronchoscopy, lung biopsy, and other diagnostic procedures. In: Murray JF, Nadel JA, Mason RJ, Boushey HA Textbook of Respiratory Medicine. Third ed. Philadelphia, PA; WB Saunders Co 2000: 725-780
  • 73 Tashkin D P, Elashoff R, Clements P J et al.. Cyclophosphamide versus placebo in scleroderma lung disease.  N Engl J Med. 2006;  354 2655-2666
  • 74 Baughman R, Strohofer S, Kim C K. Variation of differential cell counts of bronchoalveolar lavage fluid.  Arch Pathol Lab Med. 1986;  110 341-343
  • 75 Kleykamp B O, Baughman R P. Who should perform bronchoalveolar lavage analysis? [abstract].  Am J Respir Crit Care Med. 1998;  157 A178
  • 76 Poulter L W, Rossi G A, Bjermer L et al.. The value of bronchoalveolar lavage in the diagnosis and prognosis of sarcoidosis.  Eur Respir J. 1990;  3 943-944
  • 77 Welker L, Jorres R A, Costabel U, Magnussen H. Predictive value of BAL cell differentials in the diagnosis of interstitial lung diseases.  Eur Respir J. 2004;  24 1000-1006
  • 78 Agostini C, Trentin L, Zambello R et al.. CD8 alveolitis in sarcoidosis: incidence, phenotypic characteristics, and clinical features.  Am J Med. 1993;  95 466-472
  • 79 Leatherman J W, Michael A F, Schwartz B A, Hoidal J R. Lung T cells in hypersensitivity pneumonitis.  Ann Intern Med. 1984;  100 390-392
  • 80 Ando M, Konishi K, Yoneda R, Tamura M. Difference in the phenotypes of bronchoalveolar lavage lymphocytes in patients with summer-type hypersensitivity pneumonitis, farmer's lung, ventilation pneumonitis, and bird fancier's lung: report of a nationwide epidemiologic study in Japan.  J Allergy Clin Immunol. 1991;  87 1002-1009
  • 81 Baughman R P, Hurtubise P E. Systemic immune response of patients with active pulmonary sarcoidosis.  Clin Exp Immunol. 1985;  61 535-541
  • 82 Smith P A, Kohli L M, Wood K L, Hage C A, Twigg III H L, Knox K S. Cytometric analysis of BAL T cells labeled with a standardized antibody cocktail correlates with immunohistochemical staining.  Cytometry B Clin Cytom. 2006;  70 170-178
  • 83 Auerswald U, Barth J, Magnussen H. Value of CD-1-positive cells in bronchoalveolar lavage fluid for the diagnosis of pulmonary histiocytosis X.  Lung. 1991;  169 305-309
  • 84 Chollet S, Soler P, Dournovo P, Richard M S, Ferrans V J, Basset F. Diagnosis of pulmonary histiocytosis X by immunodetection of Langerhans cells in bronchoalveolar lavage fluid.  Am J Pathol. 1984;  115 225-232
  • 85 Zompi S, Couderc  LJ, Cadranel J et al.. Clonality analysis of alveolar B lymphocytes contributes to the diagnostic strategy in clinical suspicion of pulmonary lymphoma.  Blood. 2004;  103 3208-3215
  • 86 Phadke S M, Chini B A, Patton D, Goyal R K. Relapsed non-Hodgkin's lymphoma diagnosed by flexible bronchoscopy.  Pediatr Pulmonol. 2002;  34 488-490
  • 87 Poletti V, Romagna M, Allen K A, Gasponi A, Spiga L. Bronchoalveolar lavage in the diagnosis of disseminated lung tumors.  Acta Cytol. 1995;  39 472-477

Robert P BaughmanM.D. 

Division of Pulmonary and Critical Care Medicine, University of Cincinnati Medical Center

231 Bethesda Ave., Cincinnati, OH 45267-0565

Email: bob.baughman@uc.edu

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